PH.D. COURSE IN ENVIRONMENTAL SCIENCES
D
ISPERSAL AND POPULATION REGULATION OF
THE RED SWAMP CRAYFISH
(Procambarus clarkii)
R
ICARDO
M
ANUEL
O
LIVEIRA
R
AMALHO
Supervisor: Prof. Doutor Pedro Manuel Gentil Anastácio
2012 University of Évora
Department of Landscape, Environment and Planning IMAR – Institute of Marine Research
University of Évora
Department of Landscape, Environment and Planning IMAR – Institute of Marine Research
PH.D. COURSE IN ENVIRONMENTAL SCIENCES
D
ISPERSAL AND POPULATION REGULATION OF THE RED
SWAMP CRAYFISH
(Procambarus clarkii)
R
ICARDO
M
ANUEL
O
LIVEIRA
R
AMALHO
Supervisor: Prof. Doutor Pedro Manuel Gentil Anastácio
“It is not the strongest of the species that survives, nor the most intelligent that survives. It is the one that is the most adaptable to change.”
Charles Darwin
“Since the Age of Exploration began, there has been a drastic breaching of biogeographic barriers that previously had isolated the continental biota for millions of years. We are now developing a whole new cosmopolitan assemblage of organisms across the surface of the Earth with large consequences not only for the functioning of ecosystems but also for the future evolutionary trajectory of life.”
A
CKNOWLEDGEMENTS
This Ph.D. was more than the contents of this thesis. It was a continuous process of growth, a personal path walked and to be walked, another lesson of life that ultimately contributed to what I am today. For the accomplishment of the present thesis I crossed my path with several others that in some way helped and contributed to its successful conclusion. To all of them I’m greatly thankful:
o My sincere gratitude for my supervisor Prof. Dr. Pedro Manuel Anastácio for all the support, comments, scientific reviews and suggestions till the conclusion of this thesis.
o Special thanks to Prof. Dr. William Ray McClain for all the support provided during my stay in Louisiana, for all the reviews, comments, scientific suggestions and for the friendship.
o Would like to thank Institute of Marine Research (IMAR) for all the logistic support provided.
o To Prof. Drª. Alexandra Marçal Correia, thank you.
o Have to thank the Agriculture Center from Louisiana State University, on behalf of Dr. Robert Romaire, for all the logistic (Rice Research Station) and financial support for my research developed in their crayfish experimental centre facilities. Super thanks to John J. Sonnier for all the help in the field work, logistic support in Crowley, companionship and free rides on the wild west.
o Thanks are due to Centro Operacional do Arroz (COTArroz) and Associação de Beneficiários da Obra de Fomento Hidroagrícola do Baixo Mondego (ABOFHBM) for the permission to develop part of the research in their experimental rice fields.
o Quero agradecer ao Abílio, Fernanda e Ana Rita pela preciosa ajuda no processamento do material colhido no campo.
o À minha família, Mãe, Pai e Irmã por todo o apoio tantas vezes não retribuído. Sem vocês não seria o que hoje sou.
o Aos meus avós, por serem a origem de todas as coisas.
o Mena, thank you for all the Love you brought to my life. This thesis is also yours… I couldn’t finish it without you.
o À minha avó, porque ainda tem o congelador cheio de lagostins!
o That special Thank You for all my Friends, for being my life. You know who you are…
o À Raquel…sim, por isso e outras coisas.
o Special thanks to Kookie that accompanied me so many times in the field work and in all my lonely travels.
o Would like to thank all of those that contributed in any way to my thesis and I don’t have the opportunity to thank individually here.
o …aos U2!
The work included in this PhD thesis was funded by:
PhD scholarship SFRH/BD/19373/2004; Project POCTI/BSE/46862/2002 and Project DID (Dispersal of Invasive Decapods) PTDC/BIA-BEC/105182/2008
União Europeia – FEDER
A
BSTRACT
The main objective of the present thesis was to contribute to the improvement of the knowledge about red swamp crayfish (Procambarus clarkii), an exotic invasive species in Iberian Peninsula.
The main conclusions of this thesis were:
• Population density had a significant negative effect on juvenile crayfish growth;
• A learning coefficient was determined that can provide an useful tool to evaluate and compare the learning capabilities of different freshwater predators;
• M. salmoides revealed prey switching towards P. clarkii and this may be an indication
of its potential for population regulation in crayfish recently invaded areas;
• Population density significantly affected underwater P. clarkii dispersal. Other factors involved were the water temperature and period of the day;
• One of the main factors inducing P. clarkii overland dispersal was the drainage of the study area. Other variables that significantly influenced the overland dispersal of P.
“Each invasion has a certain degree of specificity. Yet, generalities are emerging yielding encouraging insights into how invasions operate and how they may be best addressed by conservation managers and policymakers. Although complicated by economic, social, and political concerns, IAS policy decisions must also be based on clear, scientific reasoning.”
R
ESUMO
D
ISPERSAO E REGULAÇAO POPULACIONAL DO LAGOSTIM-
VERMELHO-
DA-L
OUISIANA(P
ROCAMBARUS CLARKII)
O objetivo principal da presente tese foi contribuir para o aumento do conhecimento acerca do lagostim-vermelho-da-Louisiana (Procambarus clarkii), uma espécie alóctone invasora na Península Ibérica.
As principais conclusões da presente tese foram:
• A densidade populacional teve um efeito negativo significativo sobre o crescimento de lagostins juvenis;
• Foi proposto um coeficiente de aprendizagem que pode constituir uma ferramenta útil para avaliar e comparar as capacidades de aprendizagem de diferentes predadores aquáticos;
• O achigã demonstrou apresentar prey-switching sobre o P. clarkii, e este facto pode ser indicador do seu potencial para regular populações de lagostim em áreas recentemente invadidas;
• A densidade populacional teve um efeito significativo sobre a dispersão do P. clarkii dentro de água;
• A drenagem da área de estudo constituiu um dos principais despoletadores da dispersão terrestre do lagostim. A temperatura, a humidade relativa e o período do dia foram outras variáveis ambientais que influenciaram significativamente a dispersão terrestre do P. clarkii.
T
ABLE OF
C
ONTENTS
ACKNOWLEDGEMENTS ...vii
ABSTRACT ... ix
RESUMO ... xi
TABLE OF CONTENTS ... xiii
CHAPTER 1 General Introduction ... 1
1. Introduction ... 3
2. Meet the red swamp crayfish (Procambarus clarkii, Girard 1852) ... 5
3. In this thesis ... 8
4. References ... 13
CHAPTER 2 Effects of density on growth and survival of juvenile red swamp crayfish, Procambarus clarkii (Girard), reared under laboratory conditions ... 27
CHAPTER 3 Crayfish learning abilities: how does familiarization period affects the capture rate of a new prey item? ... 49
CHAPTER 4 An effective and simple method of marking crayfish ... 65
CHAPTER 5 Capture rate and crayfish movements among experimental crayfish production ponds ... 75
CHAPTER 6 Factors inducing invasive crayfish (Procambarus clarkii) overland dispersion ... 89
CHAPTER 7 General Discussion ... 121
1. General Discussion ... 123
2. Major Conclusions ... 129
A
PPENDIXAPPENDIX 1
Naïve fish learning abilities: how does learning period affects the capture rate of a new prey item? ... 137
APPENDIX 2
Predatory relations between three invasive species in Iberian Peninsula: does
prey-switching occur? ... 143
APPENDIX 3
Preliminary assessments of capture rate and crawfish movement in a commercial crawfish pond ... 149
APPENDIX 4
Assessing the efficacy of releasing crawfish back to the pond for further growth ... 157
APPENDIX 5
Invasive crayfish dispersal: the effect of population density ... 163
“Learning to identify invaders in advance would tell us a great deal about how life history traits evolve and how biotic communities are assembled. In practical terms, it could reveal the most effective means to prevent future invasions.”
C
HAPTER
1
General Introduction
“Nowadays we live in a very explosive world, and while we may not know where or when the next outburst will be, we might hope to find ways of stopping it or at any rate damping down its force.”
1. Introduction
The invasion of habitats by exotic species poses one of the major threats to biodiversity (Vitousek et al. 1997). Human activities are amongst the main reasons for the alterations of the natural range of species by the artificial translocation of many species from their natural distribution ranges, where they may establish and have substantial ecological effects on the native species communities (Mack et al. 2000; Clavero and García-Berthou 2005; Stigall 2010). In the past decades, it has become clear to scientists and policy-makers that the deliberated or accidental introduction of species (microbes, fungi, plants and animals, including genetically modified organisms) into new areas outside their native geographic distribution is one of the main drivers of biodiversity change (Sala et al. 2000). This is particularly true when the effect of the breakdown of isolating barriers between biogeographical provinces is cumulative with the shrinking of the natural areas that accommodate wild species (Rosenzweig 2001). The native distribution of the species changed, and the world changed accordingly (Mooney and Cleland 2001). Changes in the natural distribution of species should not, in general, be viewed as abnormal events since they may be considered a commonplace in nature, often occurring over the course of geological times in association with climate change (Graumlich and Davis 1993; Lodge 1993). Only stochastic events (e.g. associated with unusual climatic conditions such as storms) may induce the natural dispersal of species to habitats previously beyond their natural dispersal capabilities (MacIsaac et al. 2001). Nevertheless, human actions are more frequent and can have wider impacts. Those impacts have greatly increased the spatial and temporal rate at which species disperse and the distances they travel. By these means exotic species are able to accomplish in a few decades something that could have never been accomplished by the means of natural events alone (Lodge 1993). The World is global and an increasingly higher number of people are, nowadays, traveling faster and farther, and more goods and materials are being traded among nations and continents (Pimentel et al. 2002), creating what could be called as a
New Pangaea for some species (McKinney 2005). All these factors combined have facilitated
the introduction and expansion of non-indigenous species (NIS) in several ecosystems (Vitousek et al. 1997) and it is estimated that over 480,000 NIS have been introduced (Pimentel
et al. 2002).
Invasive NIS are a global concern, sometimes raising health issues and frequently having irreversible consequences on natural ecosystems. NIS can alter ecosystems by changing the roles of indigenous species (IS), disrupting evolutionary processes and causing significant changes in species abundance (Sala et al. 2000; Williams 2001; Lodge and Shrader-Frechette 2003). Ultimately IS will be less capable to resist and will decline, while invasive NIS will thrive (McKinney 2005). Their impact may be continuously increasing over time, even when their introduction ceases. Impacts of NIS species are diverse and, in fact, several introduced NIS
can be beneficial to humans. Species such as corn, wheat, rice, plantation forests, domestic chicken, cattle, among others, provide now more than 98% of the world’s food supply (Ewel et
al. 1999, Pimentel et al. 2002). Many NIS cause minimal environmental impact, as predicted by
the often cited tens rule. It states that approximately 10% of the imported species will escape or be introduced in the wild, 10% of which will establish themselves and 10% of the established NIS will become damaging pests (Williamson and Fitter 1996). Not all NIS have deleterious effects and the same species may have significant effects in some areas and negligible ones in others (Byers et al. 2002). For example, it is currently accepted that climate change can exacerbate the establishment and range expansion of many invasive NIS (Thomas et al. 2003; Hellmann et al. 2008). The proportion of the introduced NIS that can cause problems can be rather small, but their impact can be very serious. These species spread from the point of introduction and are often able to dominate IS populations and communities (Kolar and Lodge 2001). They may profoundly and adversely affect indigenous species, ecosystem processes, economic interests, and public health (Ricciardi et al. 1998). In one word, they may turn out to be invasive (Lockwood et al. 2007). The costs they inflict form a hidden but onerous tax on many goods and services and the damages they cause are often irrevocable. Biological invaders act as biological pollutants that, unlike chemicals, reproduce and spread autonomously, over great distances, and can adapt to changing conditions (Gherardi 2007).
Crayfish are a group of invaders outside their native geographic distribution with particularly important ecological effects (Holdich 2002). Freshwater crayfish are an important component of the aquatic fauna, frequently being the largest invertebrate predator in their habitats. They are considered both key-species and ecosystem engineers (Statzner et al. 2003; Creed and Reed 2004). Crayfish have been introduced worldwide by deliberated translocations and stocking for diverse reasons such as economic interests, aquaculture production, biological control, reduction of aquatic vegetation and aquarium hobbyists (Holdich and Lowery 1988; Henttonen and Hunner 1999; Holdich 2002). Invasive crayfish largest sphere of action are the European inland waters, where a considerable reduction of native crayfish population occurred in the 19th century mostly due to crayfish plague, an infection caused by the oomycete
Aphanomyces astaci (Holdich and Lowery 1988; Holdich 2002). There are several other
negative factors affecting native crayfish populations – e.g. habitat alterations, water pollution, habitat and shelter losses, genetic pollution, introduction of non-indigenous crayfish and subsequent competition with non-native species, predation, overfishing (Gutiérrez-Yurrita et al. 1999; Aquiloni et al. 2010). In addition, climate alterations also negatively affect native crayfish populations (Diéguez-Uribeondo 2006). One reason for the introduction of non-indigenous crayfish in Europe was the crayfish plague resistant substitutes for indigenous crayfish that should repopulate depleted benthic habitats. Unfortunately, the risks and threats associated with
such non-native crayfish species introductions into European freshwater ecosystems were generally not previously accessed and, in most cases, are now beyond control (Holdich et al. 1999a).
Once established, invasive crayfish species can eradicate indigenous crayfish and reduce populations of food items such as fish, gastropods, algae, and macrophytes, which can have cascading trophic effects elsewhere in the ecosystem (Holdich 2002). Furthermore, the indigenous crayfish species can be displaced through direct competition for the resources available and other interactions with non-invasive crayfish species (Gherardi 2006). Sympatric crayfish species compete for limited resources such as food, shelter and space and larger crayfish routinely win competitive interactions with smaller crayfish species (Momot 1984). Invasive non-indigenous crayfish species are very well equipped for competition with indigenous crayfish species due to several intrinsic characteristics (e.g. early maturation, high fecundity, high growth rate and higher levels of activity and aggressiveness) (Lindqvist and Huner 1999). They show high tolerance towards extreme environmental conditions (including chemical pollution, high temperatures, and drought) and resistance to parasites and diseases (Scalici and Gherardi 2007). In addition to the ecological effects of invasive non-indigenous crayfish introduced into Europe, some species (e.g. Orconectes limosus, Rafinesque 1817;
Pacifastacus leniusculus, Dana 1852; Procambarus clarkii, Girard 1852) are known to carry the
crayfish plague pathogen (Aphanomyces astaci Schikora) and function as vectors of the disease to the indigenous crayfish population (Vogt 1999; Holdich 2003).
The spread of non-indigenous crayfish species are therefore amongst the most important threats for indigenous crayfish species in Europe (Füreder et al. 2006) and the Iberian Peninsula is no exception. It is also important to notice that the Iberian Peninsula is included in one of the two main centres of biodiversity in the Mediterranean region hotspot of biodiversity (Médail and Quézel 1999). For this reason, improving the quality of the information about invasive non-indigenous crayfish species (e.g. distribution, life cycle, ecology) is of extreme importance to properly access their invasive potential and develop effective management strategies to control and/or supress their continuously spreading, ultimately contributing to the conservation of the native crayfish species (Aquiloni et al. 2010).
2. Meet the red swamp crayfish (Procambarus clarkii, Girard 1852)
The red swamp crayfish, Procambarus clarkii, is a relatively large – mean total length averaging 12-13 cm (Anastácio et al. 2009) and up to a maximum of 19 cm (Correia 1995) in Portuguese populations – burrowing, temperate freshwater crayfish species. Its native distribution is comprised between north-eastern Mexico and south-central USA (Hobbs 1989).
From its natural range, P. clarkii was successfully introduced into the western and eastern USA (Hobbs et al. 1989; McClain et al. 2006). This species has also been widely introduced in other countries and its current distribution comprises all continents, except Australia and the Antarctic (Hobbs 1989; Campos and Rodríguez-Almaraz 1992; Holdich et al. 1999b; Rodríguez and Suárez 2001; Campos 2005; Gherardi 2006; Harlioğlu and Harlioğlu 2006; Wizen et al. 2008). Its translocation has been mainly motivated for aquaculture purposes because this species is a popular dining delicacy (e.g. in the USA) (Gherardi 2006; McClain et al. 2006). Additionally, attempts have been made to use P. clarkii as a biological control organism in Africa since it has been experimentally demonstrated that this crayfish species is an active predator of the schistosome transmitting snails (Hofkin et al. 1991; Mkoji et al. 1999a,b).
The success of P. clarkii introductions is attributable, as mentioned before to many other invasive non-indigenous crayfish species, to factors such as its resistance to the crayfish plague, its R- reproductive strategy that comprises a short life-history, high plasticity and high fecundity rate, tolerance to extreme environmental conditions (e.g. brackish water conditions, high temperatures, dry periods, and low dissolved oxygen environments) and its ability to use a wide spectrum of food (Paglianti and Gherardi 2004; Campos 2005; Gherardi 2006; ISSG 2007; Scalici et al. 2009). Taking into account the previously mentioned ecological characteristics, P.
clarkii is considered one of the most plastic species of the order Decapoda (Lodge et al. 1998;
Campos 2005; ISSG 2007). Likewise, it is also looked upon as a keystone species that might modify the nature of native plants and animal communities (Correia 2001; ISSG 2007; Correia and Anastácio 2008).
The first record of P. clarkii in Europe was registered in the Iberian Peninsula in 1973, in the Guadiana river basin – province of Badajoz, and in 1974, in the Guadalquivir river basin – near Sevilla, where it was introduced for aquaculture purposes (Habsburgo-Lorena 1978). In less than 20 years from this first introduction, new populations of P. clarkii have been reported in at least 13 European countries (Figure 1) (Souty-Grosset et al. 2006).
In Portugal, the red swamp crayfish was reported for the first time by Ramos and Pereira (1981) in the Guadiana River basin (southern Portugal) and resulted from the natural expansion of Spanish populations (Correia 1993b). Since then, the Portuguese populations of P.
clarkii have increased very quickly due to the abundance of warm, shallow wetlands and
agricultural areas (Correia 1995) combined with the ecological plasticity of the species (Gherardi 2006). P. clarkii severe impacts on ecosystem structure and biodiversity and on rice cultures have been extensively documented (e.g. Anastácio and Marques 1997; Gutiérrez-Yurrita et al. 1998; Anastácio et al. 2000; Anastácio et al. 2005a,b; Cruz et al. 2006; Cruz and Rebelo 2007). Nowadays it has a wide distribution in the country, where it seems to be well adapted to water reservoirs and wetlands such as rice fields (Correia 1993a,b; Ilhéu and
Bernardo 1993a,b). In both countries (Spain and Portugal), soon after introduction, crayfish populations increased without control (Habsburgo-Lorena 1978; Correia, 1993b). Although it is considered an invasive species in Europe, P. clarkii is already widespread and dominant – a stage V invasive species according to Colautti and MacIsaac (2004) – and should be considered as being already naturalized, at least in the Iberian Peninsula (García-Berthou et al. 2007). Unfortunately the Mediterranean region, housing many endemic species, has been especially susceptible to species invasions and Portuguese freshwater ecosystems have suffered numerous successful introductions (Cruz and Rebelo 2007; Ribeiro and Collares-Pereira 2010; Rebelo et
al. 2010). Although the ecological impacts of these introductions are still poorly documented,
they have been implicated in the decline of native freshwater fauna (Cabral et al. 2006).
Figure 1. Current distribution of Procambarus clarkii in Europe. Portugal, Spain, France and Italy have
the majority of the populations (adapted from Souty-Grosset et al. 2006).
Its intense burrowing inflicts structural damages to the banks of rivers and lakes (Barbaresi et al. 2004b) and causes water bioturbation leading to a reduction in primary productivity (Gherardi 2007). P. clarkii is an important pest in rice fields because it destroys levees and consumes young rice plants (Sommer and Goldman 1983; Grigarick 1984; Sommer 1984; Correia 1993b; Anastácio and Marques 1997; Anastácio et al. 2000). It is well known that, just after its introduction, when populations are rapidly growing, P. clarkii has dramatic effects on the community by depleting all food sources available because of its voracity and ability to shift its diet (Huner and Barr 1991; Ilhéu and Bernardo 1993a,b; Gutiérrez-Yurrita et
al. 1998). Nevertheless, it is possible to increase the profits of rice-farmers by double cropping
rice (Oryza sativa) and red swamp crayfish as it has been done intensively in the USA (Chien and Avault 1980; McClain et al. 2006). Like in other places P. clarkii introduction in Portugal became a problem for rice farmers (Anastácio and Marques 1997; Anastácio et al. 2005a,b). To prevent damage to rice crops, farmers tried to eliminate crayfish by means of xenobiotic chemicals. This had a strong negative effect in the environment and did not solve the problem. In fact, once introduced into favourable habitats, P. clarkii is difficult to eliminate (Holdich and Lowery 1988). A better solution could be the use of crayfish as a food resource, which would control the size of crayfish populations, with a simultaneous socio economical profit (Chien and Avault 1980; McClain et al. 2006). Nevertheless, caution should be taken since it can accumulate heavy metals (Gherardi at al. 2002a) and toxins from microalgae (Tricarico et al. 2008).
P. clarkii outcompetes indigenous crayfish species (e.g. Astropotamobius pallipes)
being dominant in aggressive interactions (Gherardi and Cioni 2004) and transmitting the oomycete Aphanomyces astaci (Diéguez-Uribeondo and Söderhäl 1993). Due to its voracious feeding habits and high densities achieved, P. clarkii is today recognized to be a cause of biodiversity loss in the invaded water bodies (Correia and Anastácio 2008). It causes the local extinction of various species of molluscs, fish, amphibians and hydrophytes (Cruz et al. 2006; Gherardi et al. 2001; Renai and Gherardi 2004; Gherardi and Acquistapace 2007). There is a negative relationship between P. clarkii abundance and the distribution and abundance of floating leaved and submerged aquatic plants (Harper et al. 2002) as well as a so-called special relationship with water hyacinth (Eichornia crassipes) being associated with the significant reduction of this macrophyte in the water bodies (Foster and Harper 2006). The consequences of the introduction of P. clarkii on Portuguese riverine and aquatic communities are still poorly understood, although some studies have documented its role as a prey of diverse avian, mammal and fish (see Godinho and Ferreira 1994; Beja 1996a,b; Correia 2001) and also its trophic preferences (Ilhéu and Bernardo 1993b; Foster and Slater 1995; Ilhéu and Bernardo 1995; Gutiérrez-Yurrita et al. 1999; Anastácio et al. 2011). It is important to mention that P. clarkii is an important component of the diet of endangered and emblematic species in Portugal, such as the otter (Luttra luttra) and the white stork (Ciconia ciconia) (Beja 1996a,b; Correia 2001).
3. In this thesis
Since Charles Elton (1958) seminal book, ecologists have tried to predict and control the distribution and spread of non-indigenous species. It seems that a key factor regulating species invasion is opportunity: the more frequently and persistently a foreign plant or animal is exposed to a new environment, the better are its odds of invading it (Davis 2009). Several
studies modelled the distribution and the deleterious effects of non-indigenous crayfish species on ecosystems, however such studies often requires that a large amount of quantitative information is available. Understanding the spatial and temporal distribution of species, and invasive species in particular, requires profound knowledge of the limiting factors (biotic and abiotic) regulating species distribution (Davis 2009).
Understanding the environmental factors determining the establishment and colonization of new areas by the invasive populations is a crucial issue in the study of biological invasions. Knowledge of these variables and the factors determining them can be used to elaborate risk assessment maps for other invasive species, in order to define high-risk areas susceptible to invasion. In fact, an important approach to prevent further invasions is predicting the potential outcome of introductions on the basis of the knowledge of ecological requirements of potential invaders. Because of the severity of the impacts of biological invasions and the difficulty of eradicating an exotic species once it has established, it is pivotal to develop prospective work allowing the detection of invasions in their initial stages (Zalba et al. 2000).
Crayfish growth is affected by several variables such as: water temperature, water quality, food availability, light intensity, photoperiod, crayfish length and density, among others (e.g. McClain et al. 1992; Nyström 1994; Gutiérrez-Yurrita and Del Olmo 2004; Paglianti and Gherardi 2004). The negative effect of crowding or, in other terms, population density, on growth has been previously reported (Lutz and Wolters 1986; Jarboe and Romaire 1995). However, in these studies the highest densities tested were rarely above 20 individuals m-2. Thus, there is a lack of knowledge on the response of red swamp crayfish to population density at higher densities and further research is needed in order to quantify and determine the extent of such effects, in spite of food availability. This knowledge is especially relevant for juvenile production facilities because it helps to understand the reactions of crayfish to overcrowding. The determination of growth parameters is also relevant for the management of wild population, especially in invaded areas. The density regulation of growth is a form of intra-specific population regulation. There is a lack of knowledge on the response of red swamp crayfish, particularly of the early stages of development, to population density under controlled laboratory conditions at high densities and a laboratory experiment was conducted in order to determine and quantify such effects (Chapter 2).
Learning abilities are fundamental for survival and, in any ecosystem, prey animals are required to learn to recognize certain predatory cues of potential predators. This has been demonstrated, for example, in fish (Karplus et al. 2006; Siebeck et al. 2009), damselflies (Chivers et al. 1996; Wisenden et al. 1997) and crayfish (Hazlett and Schoolmaster 1998). Invasive crayfish exhibit a high degree of plasticity in learning to reduce predation risk (Hazlett 2000), and some species (e.g. Orconectes virilis and P. clarkii) seem to learn to avoid predation
quicker than native species (Gherardi et al. 2002b; Hazlett et al. 2002). This characteristic constitutes an important adaptive advantage when invading a new habitat (Acquistapace et al. 2003). Learning to quickly recognize new prey items will also substantially increase the invader predator fitness. Crustaceans are important predators in many ecosystems and their learning plasticity has been demonstrated both on crabs (Roudez et al. 2008) and invasive crayfish. In fact, invasive crayfish have the ability to readily switch to new prey items in contrast to native crayfish species (Gherardi et al. 2001). The plasticity of crayfish for learning to recognize new prey may provide important insights about the potential success of a species when invading new habitats. Several studies have reported evidence of learning in a variety of arthropod species (Papaj and Prokopy 1989; Dukas 2008; Ishii and Yamada 2010), however, the application of equations and mathematical modelling to the learning processes is not common. A study was conducted to determine whether prior experience influences the success rate of prey capture and to estimate and mathematically explain the learning curve of P. clarkii as a naïve predator (Chapter 3).
When an area is recently invaded, the invader often encounters other invasive species already established and the invasion process is the result of the inter-specific interaction between both native and non-native species. As an attempt to manage invasive species studies focusing on invasive species in both natural and humanized ecosystems have been carried out (Simon and Townsend 2003). There are some studies about the inter-specific consumption and influence of P. clarkii on aquatic biocenoses (Correia 2002, 2003; Correia et al. 2005; Anastácio et al. 2011) but not much information is available about the effects of other predators (e.g. fish) over P. clarkii populations. As stated above for P. clarkii learning also plays an important role when considering fish predators (Karplus et al. 2006; Siebeck et al. 2009). An experiment was conducted (Apendix 1) with the objective of determine the effect of learning time on the predation of P. clarkii by the largemouth bass (Micropterus salmoides), a non-native invasive fish predator in the Iberian Peninsula inland waters (Godinho and Ferreira 1998).
Prey-switching in predators, which attack several prey species, can potentially stabilize prey populations numbers (Murdoch 1975; Nilsson 2001; Palomino-Bean et al. 2006). When switching occurs, the number of attacks upon a species is disproportionally large when the species is abundant relative to other prey and disproportionally small when the species is relatively rare. Although several other factor may be involved in prey population regulation (e.g. prey and predator size, environmental conditions). This process may be important when considering the regulation of invasive crayfish species. Detailed information and mathematical approaches to the interspecific relation between P. clarkii and other invasive species are scarce, particularly regarding prey switching among its fish predators. Understanding of switching in natural systems will requires detailed research of the behavioural mechanisms in the response of
predator preference to changes in prey density (Abrams and Matsuda 2004). This is important to provide new insights on the processes and mechanisms of invasion and its effects on invaded aquatic biocenoses (Marco et al. 2002). Attempts were conducted to access the occurrence of prey switching in a system with three invasive species, involving P. clarkii and two fish species,
Micropterus salmoides and mosquitofish (Gambusia holbrooki) (Apendix 2).
There are several different marking methods successfully used in mark-recapture experiments, each of them with its advantages and disadvantages (e.g. visible implant elastomers, visible implant alphanumeric tags, radio-telemetry, uropod clipping among others) (Abrahamsson 1965; Guan 1997; Guan and Wiles 1999; Gherardi and Barbaresi 2000; Robinson et al. 2000; Bubb et al. 2002; Gherardi et al. 2004; Bubb et al. 2006; Clark and Kershner 2006; Mazlum 2007; Kuhlmann et al. 2008). The choice of the technique to be used will depend on the theoretic and management question, the behaviour of the species, the habitat it inhabits and the available resources (economic and logistic constraints). During the present research a simple, cheap and effective (for our objectives) marking method was developed (Chapter 4). This method made it easier to proceed with several field and laboratory work programmes described in this thesis.
The identification of the initial locus of invasive non-indigenous species and their route of invasion is of great theoretical and practical importance (Wilson et al. 1999; Kreiser et al. 2000). Migration and dispersion1 may be critical, not only for the continuity of the propagule pressure, but also as an important source of genetic variation necessary for the adaptative evolution (Etterson and Shaw 2001) of the invasive population. Crustacean dispersal behaviour evolved for the displacement of the animal in space (Herrnkind 1983). Although the world-wide spread of P. clarkii is mainly attributed to human introductions (Gherardi et al. 2006), the rapid and widespread expansion of the species, following its establishment, is the result of its active dispersal capabilities. The ability to disperse overland enables a freshwater species to colonize new water bodies in the neighbourhood and it is known that P. clarkii has the ability to exit the water and move overland (Penn 1943; Holdich 2002; Kerby et al. 2005; Cruz and Rebelo 2007; Chucholl 2011). P. clarkii can resist drought by burrowing until the next rainy season (Huner and Barr 1991) or use overland dispersion to move to a larger pool or one with more favourable conditions (Penn 1943; Aquiloni et al. 2005). P. clarkii population dynamics is well documented in the Iberian Peninsula (Correia 1995a,b; Gutiérrez-Yurrita et al. 1999; Ligas 2007; Gherardi 2006; Alcorlo et al. 2008; Anastácio et al. 2009) and some studies have explored its underwater dispersal abilities (Gherardi and Barbaresi 2000; Gherardi et al. 2000; Aquiloni et al. 2005) Nevertheless, little is known about P. clarkii ability to disperse overland
1
In the context of this thesis dispersal is considered as the active or passive spreading of individuals away from others (e.g. from an existing populations or form their inicial location). Migration, on the other hand, is an active and
and colonize new freshwater areas and the factors involved in its overland dispersal remains unclear and not quantified. Some studies were conducted in order to characterize P. clarkii overland dispersion and determine the main environmental triggers involved (Chapter 5, Chapter 6 and Apendix 3).
Considering P. clarkii plasticity and invasive potential, particularly its high resistance to adverse conditions and behavioural adaptations, this species provides an excellent opportunity to analyse how behaviour contributes to its invasive potential in European ecosystems. One of the objectives of this thesis was to identify the factors involved in P. clarkii’s seasonal overland dispersion, so that in the future, more efficient predictions of the spread in invaded areas can be obtained and more effective management or exploitation is possible. It has also been reported that crayfish behaviour changes with population density (Bovbjerg and Stephen 1975; Holdich 2002) and some studies (e.g. Bovbjerg 1959) support the hypothesis that crayfish underwater dispersion increases with population density. An experiment was set to determine whether density influences P. clarkii underwater movement (Apendix 5).
The crayfish aquaculture industry of the USA is located primarily in Louisiana where over 1,100 producers cultivate procambarid crayfish on over 70,000 ha, producing in excess of 44,000 metric tons worth over $100 million USD annually (LCES 2009). The sole method used for harvest of procambarid crayfish from aquaculture ponds in the Southern USA is the baited wire-mesh trap. Baited trap efficiency is dependent on a number of variables, such as crayfish density, bait type, trap soak interval, and environmental factors. However, the efficiency of the standard trapping protocol to remove harvest size crayfish from a population has not been thoroughly examined. Baited traps are often used to determine crayfish population parameters and the trap efficiency may significantly influence the results os such assessments (Acosta and Perry 2000). On the course of the present thesis some attemps were conducted to determine the capture rate and efficacy of baited traps in Louisiana production systems (Chapter 5, Apendix 3 and Apendix 4).
Detailed data regarding the inter- and intra-specific population regulatory mechanisms, migratory ability, seasonal migrations and dispersal, learning abilities and interaction with sympatric predators are missing for P. clarkii. The increase of the knowledge about invasive species is crucial to develop detailed and more accurate models in order to manage the existing populations and provide tools that may contribute to a future predictor of the impacts of these species in nature. In the present thesis detailed information about P. clarkii was collected in order to contribute to increase the knowledge regarding this invasive species. Ultimately, this information can be integrated in mathematical models that would contribute significantly to the understanding of the invasiveness of crayfish species. These could also be used to manage the
existing naturalized populations, to control or predict future suitable areas and to minimize the impacts in non-indigenous species in the ecosystem and in the economy.
The main objectives of the research within this thesis were:
• Evaluate intra-specific population regulation, namely the importance of population density on growth and survival of young of the year P. clarkii, and to understand the effects of density on both the period between moults and the length increment between moults without food limitation;
• Determine crayfish learning abilities, in terms of their capacity to learn how to prey on new preys;
• Evaluate the possibility of inter-specific population regulation, namely the influence of learning on P.clarkii capture rate by the largemouth bass (Micropterus salmoides) and the occurrence of prey-switching in a three invasive species system.
• Study and characterize P. clarkii dispersion, particularly the post-reproductive dispersion and determine the environmental triggers involved in P. clarkii overland dispersal;
• Determine the effects of population density on P. clarkii underwater activity;
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